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Cooksville was an important stage coach stop along the Dundas highway, which was carved out of the wilderness after a survey by Asa Danforth Jr. in 1798. The first settler was Daniel Harris, an immigrant from the United States, in 1800, so the settlement was first named Harrisville.[2]

Jacob Cook bought 100 acres (40 ha) at the southwest corner of Dundas Street and Hurontario Street for $30 in 1819 and the settlement was renamed in his honour.[2]

The entrepreneur won the contract to deliver the mail from York to Niagara, operated several stage coach lines, was the local magistrate and built the Cooksville House, the first licensed tavern in the area at the northwest corner of Dundas and Hurontario streets in 1829.[2] A heritage Mississauga sign on Hurontario Street north of the intersection claims it was the first Canadian location of winemaking in 1836.[2]

Cooksville grew in size and influence until the Great Fire of 1852 razed much of it.[2]
A severe tornado hit the area on June 24, 1923 destroying mostly rural farmhouses around the town.
On the west side of the town there was a 182 acre brickyard that sprawled south of the CP rail line from 1912 until its closure in 1995, employing many Cooksville residents over that period. The Italian Heavyweight champion boxer, Primo Carnera had worked at the yard for a short period during his youth. Today, the converted site is a medium density residential and retail zone along Shoreline Dr., just south of the infamous 1979 Mississauga train derailment site at the CP crossing (Mavis Road).

Much of the new suburban growth in Mississauga before amalgamation in the 1960s occurred in areas around Cooksville. For much of that time it had the highest concentration of high-rise condominium and rental buildings in Mississauga. In recent years it has been overtaken in density by the City Centre just to north of Cooksville and the area immediately surrounding the Square One Shopping Centre.

Cooksville is also the main transportation hub in Mississauga, with GO Transit rail and bus service and express city buses to Toronto Union Station. Cooksville GO Station is near the original corners of the settlement, and the MiWay and GO Bus Terminal is adjacent to the north parking lot of the Square One Shopping Centre to the north.

The population of the area is highly diverse with people from originating from all over the world, over half are visible minorities. There is a plethora of South Asian and Arab textile/clothing shops, restaurants and grocery stores in the area. There is also a significant number of Afro-Caribbean take-out restaurants and barber shops; the area is known to cater towards Mississauga's black community because of the large number of barber shops in close proximity to one another. Nevertheless, the area is multicultural and most cultures are represented in the area.